water

Article Passage Performance of Technical Pool-Type Fishways for Potamodromous Cyprinids: Novel Experiences in Semiarid Environments

Francisco Javier Sanz-Ronda 1,* , Francisco Javier Bravo-Córdoba 1 , Ana Sánchez-Pérez 2, Ana García-Vega 1 , Jorge Valbuena-Castro 1, Leandro Fernandes-Celestino 3 , Mar Torralva 2 and Francisco José Oliva-Paterna 2 1 Applied Ecohydraulics Group (GEA-ecohidraulica.org), E.T.S.II.AA, University of Valladolid, 34004 Palencia, ; [email protected] (F.J.B.-C.); [email protected] (A.G.-V.); [email protected] (J.V.-C.) 2 Departmento of. and Physical Anthropology, Universityof Murcia, 30100 Murcia, Spain; [email protected] (A.S.-P.); [email protected] (M.T.); [email protected] (F.J.O.-P.) 3 Group on Technology in Ecohydraulics and Conservation of Fishery and Water Resources (GETECH), Western Paraná State University (Unioeste), 85903 Toledo, Brazil; [email protected] * Correspondence: [email protected] or [email protected]

 Received: 22 October 2019; Accepted: 8 November 2019; Published: 11 November 2019 

Abstract: Endemic freshwater fish from semiarid environments are among the most threated in the world due to water overexploitation and fragmentation problems. Stepped or pool-type fishways are used worldwide to reestablish longitudinal connectivity and mitigate fish migration problems. Many of them are being installed or planned in rivers of semiarid environments, however, very few studies about fish passage performance through pool-type fishways has been carried out to date on these regions. The present work focuses on the passage performance of two potamodromous cyprinids endemic of these regions, with different ecological and swimming behavior: southern ( sclateri) and Iberian straight-mouth nase (Pseudochondrostoma polylepis). These are assessed in two of the most common types of stepped fishways: vertical slot and submerged notch with bottom orifice fishways. Experiments were carried out during the spawning season in the Segura River (southeastern Spain), using a passive integrated transponder (PIT) tag and antenna system. Ascent success was greater than 80%, with a median transit time lower than 17 minutes per meter of height in all trials, and for both species and fishway types. Results show that both types of fishways, if correctly designed and constructed, provide interesting alternatives for the restoration of fish migration pathways in these regions.

Keywords: Mediterranean region; river connectivity; fishway assessment; fish motivation; ascent ability

1. Introduction Rivers in semiarid environments are subjected to strong seasonal variability—long drought periods alternated with large but brief floods [1,2]. Thus, water resources are strongly exploited, and rivers are highly affected by barriers and flow regulation [3,4]. Transverse barriers, such as , weirs, and gauging stations, and the involved habitat fragmentation are considered the main threats to ichthyofauna worldwide [5,6], including in semiarid regions [7–9]. Moreover, near-future scenarios suggest more water demand and the exacerbation of human stressors [10,11]. In these areas (i.e., from the circum-Mediterranean region to Central Asia), freshwater fish fauna present a high degree of endemism and are characterized by a low number of families, with most of the species belonging to the [12–15]. The most abundant species are barbels ( and

Water 2019, 11, 2362; doi:10.3390/w11112362 www.mdpi.com/journal/water Water 2019, 11, 2362 2 of 14

Luciobarbus) and nases (genus Chondrostoma, Pseudochondrostoma, and Parachondrostoma). Both rheophilic potamodromous cyprinids are under different levels of threat according to the International Union for Conservation of Nature (IUCN) Red List of [4,16]. This ichthyofaunistic group is an important link for the trophic interactions within the ecosystem and inhabits the entire length of the river, migrating during the spring in order to reproduce in shallow waters with gravel and moderate current velocity [13,17]. Two representative potamodromous fish species of the Iberian semiarid region are the Southern Iberian barbel (Luciobarbus sclateri) and the Iberian straight-mouth nase (Pseudochondrostoma polylepys)[18]. Both species are common in the southern and eastern and they show different ecological traits and swimming behavior [19]. The Southern Iberian barbel is defined as a sentinel species [20] in this region, and it is a large-bodied benthic fish that lives in slow water velocity . Iberian straight-mouth nase is a medium-bodied water column fish that inhabits running waters [16]. River connectivity is an essential requirement for the effective functioning of freshwater ecosystems, and in particular for allowing fish to complete their life cycles [21,22]. The longitudinal connectivity for fish is usually restored by different types of fishways. Technical pool-type or stepped fishways are the most used designs around the world [23,24], including in semiarid regions [25–28]. Nevertheless, in northern Africa, the Eastern Mediterranean area, and Central Asia, fishways in cyprinid rivers are still very scarce [29–31]. These types of fishways consist of pools connected by cross-walls with slots, notches, and/or orifices, which divide the total height of an obstacle into smaller drops to ensure that the hydraulic conditions inside are in the range of the physical capacities of fish fauna, and thus, enable their passage [32,33]. The most common designs in the Iberian Peninsula are vertical slot (VS) and submerged notch with bottom orifice (SNBO) fishways [26,34]. On one hand, VS fishways allow fish movements at any desired depth through the slot and they tolerate variations in the upstream water levels better than SNBO, although they need more discharge than SNBO to get the same depth. In the other hand, SNBO can work with greater slopes and a wider range of design discharge, and they always ensure a minimum depth in the pool. In SNBO, the bottom orifice allows benthic fish passage, although it can be easily clogged by debris [24,32]. The suitability of both VS and SNBO has been previously probed for North American and Central European cyprinids [35], and even for some northern Iberian cyprinids, such as Iberian barbel () and northern straight-mouth nase (Psudochondrostoma duriense)[36–38]. Similar ascension and swimming behaviors are usually assumed for other species of the same genus or family, and thus fishway design criteria of one region are usually extrapolated to other river basins [24,39–41]. Nevertheless, species have evolved by adapting to different hydraulic regimens and climate conditions. Semiarid South Iberian rivers are usually more unsteady and warmer than northern ones. Fishways assessments in this region are still scarce. Hence, studying passage performance of southern fish species will provide important information about their ascent abilities, and in general will improve fishway design. Passage performance depends on the interactions between physical (geometric and hydraulic features of the fishway), biological (fish behavior, swimming ability, age, sex, physiological status), and environmental (water temperature, fishway discharge) parameters [42–45]. Standardized passage metrics based on movement theory usually consider fish ascent success, transit time, and motivation (definitions in Section 2.4) to quantify passage performance [46–48], and also to compare different types of fishways or to understand the swimming behavior of different fish species [36,38,49]. The present study focuses on the passage performance of two potamodromous cyprinids from a semiarid region of the Iberian Peninsula, Southern Iberian barbel and Iberian straight-mouth nase, in the two main typologies of pool-type fishways: VS and SNBO. Specifically, ascent success, passage time, and motivation of target fish are analyzed to determine: (1) if both types of fishways are suitable for them; (2) if there are differences in passage efficiency between fishway types and fish species; and (3) to understand the influence of hydraulic and biometric parameters on ascent metrics. This information Water 2019, 11, 2362 3 of 14 will help biologists and engineers in fishway design, implementation, and management decisions in many semiarid watercourses inhabited by species with similar behavior. Water 2019, 11, 2362 3 of 14 2. Materials and Methods 2. Materials and Methods 2.1. Study Area and Experimental Sites 2.1. Study Area and Experimental Sites The Segura Basin, in the southeast of Spain, is one of the most arid European regions, with an averageThe annual Segura temperature Basin, in the of southeast 18 ◦C, scarce of Spain, rainfall is (approximately one of the most 300 arid mm European/year), and regions, intense with surface an andavera groundwaterge annual temperature overexploitation of 18 for°C, irrigationscarce rainfall [50]. (approximately The experiments 300 were mm/year), carried and out intense in two fishwayssurface and located groundwater in the middle overexploi part oftation the Segura for irrigation River: VS [50]. in the The El experiments Jarral weir (Universal were carried Transverse out in Mercatortwo fishways –UTM-Grid located Zone in the 30 North;middleEuropean part of the Terrestrial Segura ReferenceRiver: VS Systemin the 1989El Jarral -ETRS weir 89-, (Universal X: 640577, Y:Transverse 4229308; Abar Mercatorán, Murcia) –UTM- and Grid SNBO Zone in 30 the North; post-trasvase European weir Terrestria (UTM30l ETRSReference 89, X: System 613788, 1989 Y: 4235661; -ETRS Calasparra,89-, X: 640577, Murcia) Y: 42293 (Figure08; Abarán,1). Both Murcia) fishways and are SN placedBO in inthe small post-trasvase weirs for weir combined (UTM30 irrigation ETRS 89, and X: hydropower613788, Y: 4235661; production. Calasparra, The distance Murcia) between (Figure them 1) is. Both 44.7 kmfishways and they are share placed similar in small environmental weirs for characteristicscombined irrigation (flow discharge,and hydropower substrate, production. vegetation, The and distance fish population). between them In theis 44.7 study km reach, and they the Segurashare similar River has environmental a catchment areacharacteristics of 8486 km 2(flo, withw adischarge, mean altitude substrate, of about vegetation, 200 m above and mean fish seapopulation). level, and In a meanthe study annual reach, discharge the Segu ofra 20.35 River m3 /hass. It a is catchment placed in thearea Epipotamon of 8486 km2 zone, with [51 a ],mean and correspondsaltitude of about to E4 200 category: m above gravel mean bed sea streamlevel, and of higha mean sinuosity annual with discharge a slope of of 20.35 0.001–0.02 m3/s. It mis/ mplaced [52]. Thein the fish Epipota communitymon zone in the [51], main and stem corresponds of the Segura to E4 River category: is very gravel altered bed due stream to the of modification high sinuosity of thewith hydrological a slope of 0.001–0.02 regime for m/m irrigation [52]. The and fish the community introduction in the of main non-native stem of invasive the Segura species River [ 53is ].very In the middle part of the basin, among the most abundant potamodromous migratory species are the native southern Iberian barbel and the translocated Iberian straight-mouth nase (hereafter referred to as barbel and nase, respectively) [53].

FigureFigure 1.1.Study Study site site location: location: Segura Segura River River basin inbasin the semiarid in the regionsemiarid of theregion western of circum-Mediterraneanthe western circum- Area.Mediterranean Area.

BothBoth fishwaysfishways werewere designeddesigned andand constructedconstructed asas aa partpart ofof thethe Segura-RiverlinkSegura-Riverlink LIFE12LIFE12 ENVENV/ES/001140/ES/001140 projectproject [[54],54], followingfollowing thethe standardstandard designdesign guidelinesguidelines [[24,32]24,32] andand consideringconsidering thethe geometricalgeometrical andand hydraulichydraulic recommendationsrecommendations for cyprinidscyprinids (Figure(Figure2 2 and and Table Table1 ).1). Fishway Fishway bottoms bottoms werewere coveredcovered by by substrates substrates from from the the riverbed riverbed to to increase increase roughness, roughness, and and discharge discharge can can be regulatedbe regulated by aby sluice a sluice gate gate located located in thein the flow flow entrance. entrance. At At each each fishway, fishway, a a section section with with a a 1.80 1.80 mm headhead (di(differencefference betweenbetween thethe headwaterheadwater andand tailwatertailwater levels)levels) waswas selectedselected forfor thethe trials.trials. Water 2019, 11, 2362 4 of 14 Water 2019, 11, 2362 4 of 14

Figure 2.2. ExperimentalExperimental set-up.set-up. Black Black cross-walls: cross-walls: closing closing mesh mesh (start (start and and finish finish of the of test the section); test section); black blackcircles: circles: closing closing mesh duringmesh during adaptation adaptation period; peri meshod; overmesh the over pools: the adaptationpools: adaptation pools; dottedpools; dotted circles: circles:antennas antennas with their with position their posi numbertion number (antenna (antenna 1 -A1-, antenna1 -A1-, antenna 2 -A2-, etc.,2 -A2-, being etc., 1.80 being m, the1.80 relative m, the relativeheight between height between A1 and A1 A4 and for bothA4 for fishways); both fishways); arrows arrows indicate indicate flow and flow fish and ascent fish ascent directions. directions. Note: Note:SNBO SNBO= submerged = submerged notch notch with bottomwith bo orifice;ttom orifice; VS = verticalVS = vertical slot. slot.

Table 1. Mean geometric and hydraulic variables for the studied vertical slot (VS) and submerged Table 1. Mean geometric and hydraulic variables for the studied vertical slot (VS) and submerged notch with bottom orifice (SNBO) fishways. Range of values in brackets. notch with bottom orifice (SNBO) fishways. Range of values in brackets. Variables VS SNBO Variables VS SNBO Pool dimension (length width) 2.10 m 1.60 m 2.40 m 1.60 m Pool dimension (lengt×h × width) 2.10 m ×× 1.60 m 2.40 m × 1.60× m Slope 6.52% 7.31% Slope 6.52% 7.31% Number of pools between A1 and A4 11 8 NumberWidth of ofpools the slotbetween/notch A11 and A4 0.23 m 11 (0.20–0.23) 0.32 m 8 (0.31–0.36) HeightWidth of of the the notch slot/notch sill 1 1 0.23 m (0.20–0.23)NA 0.32 0.49 m (0.31–0.36) m (0.45–0.52) Bottom orifice size (length width)1 NA 0.20 m 0.25 m Height of the notch× sill NA 0.49 m (0.45–0.52)× Drop between pools 1 0.15 m (0.14–0.19) 0.19 m (0.13–0.24) Bottom orifice size (length × width) NA 0.20 m × 0.25 m Mean water depth 1 0.91 m 0.99 m 1 FlowDrop dischargebetween pools2 0.15 m0.29 (0.14–0.19) m3/s 0.19 m (0.13–0.24) 0.31 m3/s VolumetricMean Energy water Dissipation depth 1 118 W 0.91/m3 m(110–149) 148 0.99 W/m m3 (102–181) 3 Water velocityFlow at discharge the slot/notch 2 1.380.29 m/s (1.10–1.47)m3/s 1.240.31 m m/s3 (0.80–1.36)/s Water velocity at the orifice 3 NA 1.72 m/s (1.42–1.93) Volumetric Energy Dissipation 118 W/m3 (110–149) 148 W/m3 (102–181) 1 MeasuredWater with a velocity total station at the (model slot/notch Leica 3 TC307, 1.38 Heerbrugg, m/s (1.10–1.47) Switzerland) 1.24 or measuringm/s (0.80–1.36) tape 0.01 m; 2 Calculated with in the same manner as Fuentes-Pérez et al. [33]; 3 Direct measurements with a propeller flowmeter± 0.01 m/s (modelWater 2100, velocity Swoffer at Instruments the orifice Inc., 3 Summer, WA, USA).NA Note: NA =1.72not m/s applicable. (1.42–1.93) ± 1 Measured with a total station (model Leica TC307, Heerbrugg, Switzerland) or measuring tape ± 0.01The m; boundary 2 Calculated conditions with in the imposed same manner by theas Fuentes-Pérez river at the et entrance al. [33]; 3 Direct of the measurements fishway (water with level downstream)a propeller during flowmeter the ± trials0.01 m/s influenced (model 2100, the Sw loweroffer partInstruments of the Inc., fishway, Summer, producing WA, USA). non-uniform Note: conditionsNA = not with applicable. backwater profiles (more evident in the SNBO), increasing the water depth in the most downstreamThe boundary pools andconditions reducing imposed the water by drops, the river and thusat the obtaining entrance lower of the values fishway of water (water velocity level downstream)and energy dissipation during the [33 trials,55]. influenced the lower part of the fishway, producing non-uniform conditions with backwater profiles (more evident in the SNBO), increasing the water depth in the 2.2. Fish Capture, Tagging, and Handling most downstream pools and reducing the water drops, and thus obtaining lower values of water velocityA passive and energy integrated dissipation transponder [33,55]. (PIT) tag and antenna system was used to study fish movements. Trials were performed from 3–8 May 2017, within barbel and nase reproductive migration periods. 2.2.Fish Fish were Capture, captured Tagging, by electrofishing and Handling (Erreka model; 2000 W, 200–250 V, and 2–3 A) one day before trials in river reaches upstream of each fishway. There were unpassable barriers between the capture areas A passive integrated transponder (PIT) tag and antenna system was used to study fish and the experimental fishways. Once captured, fish were anesthetized with tricaine methanesulfonate movements. Trials were performed from 3–8 May 2017, within barbel and nase reproductive (MS-222, 0.1 g/L), measured (fork length, 0.1 cm), weighed ( 1 g), and tagged with a PIT tag (Table2). migration periods. Fish were captured by± electrofishing (Erreka± model; 2000 W, 200–250 V, and 2–3 A PIT tag is an encapsulated microchip used for radiofrequency identification (RFID). PIT tags were A) one day before trials in river reaches upstream of each fishway. There were unpassable barriers introduced into the intraperitoneal cavity of the fish through an incision posterior to the left pectoral between the capture areas and the experimental fishways. Once captured, fish were anesthetized with tricaine methanesulfonate (MS-222, 0.1 g/L), measured (fork length, ±0.1 cm), weighed (±1 g),

Water 2019, 11, 2362 5 of 14

fin [56]. As the weight of each tag must be lower than 2% of the fish weight, two sizes of PIT tags were used: 23 mm long and 3.65 mm diameter, and 12 mm long and 2.12 mm diameter (TIRIS model RI181 TRP-WRHP; Texas Instruments). This method shows negligible effects on growth, survival, and behavior of many species [57] and is very common in fish movement studies [58]. Afterwards, fish were transported in aerated water tanks (100 L) and subsequently stabled in two similar groups per fishway (mix of barbel and nase) for acclimation inside cages: groups VS1 and SNBO1 in a pool in the fishway, and groups VS2 and SNBO2 in the river near the fishway (Table2). Prior to the start of the trials, each group was confined to the initial pool (the most downstream; Figure2) by two closing mesh areas and a low fishway flow (50 L /s), to ensure adaptation and avoid stress or fatigue. Fish were not fed during experiments, although they could access natural food sources drifting into the cages or on the bottom. No fish died during or after the tagging process and trials. Fish were treated in accordance with the European Union Directive 2010/63/UE on the protection of used for scientific purposes, and following the ethical guidelines of Murcia University and the Government of Murcia, under authorization AUF20150077. All efforts were made to minimize stress, and fish were released after the experiments.

2.3. Trials A system of antennas was used in both fishways to detect the movements of the PIT-tagged fish. Four antennas were installed in each fishway at a total head of 1.80 m (Figure2), covering the slot in VS and the notch and the orifice in SNBO, with a detection range of 20 cm distance from the antenna. ± Each antenna was connected to a reader (Half Duplex multiplexer reader, ORFID®, Portland, Oregon, USA) programmed to send and receive information at 14 Hz (3.5 Hz or 0.29 s per antenna). At the start of a trial, the fishway gate was open, allowing usual operating flow (Table1), and the closing mesh in the starting pool was removed. Therefore, fish were allowed to ascend volitionally but they could not escape from the fishway due to the presence of the closing meshes in both the lower and upper zones of the experimental area (Figure2). If a fish reached the uppermost pool, it had two options: remaining there or descending. Two 16-hour trials (from 8:00 to 24:00 h) were attempted in each fishway, one for each fish group; thus, a fish participated in only one trial (Table2). Prior to trails, other fish that remained in the fishways were removed before releasing experimental individuals from each group. Water level and temperature were monitored at 30 min intervals (Orpheus Mini, OTT Hydromet GmbH, Kempten, Germany), with small variations observed during the trials (16–19 ◦C in the VS group and 14–17 ◦C in the SNBO group). The weather was sunny and cloudless during the experiments.

Table 2. Fish samples.

Length (cm) Weight (g) K Fish Group Species N Mean SD Range Mean SD Range Mean SD Range ± ± ± Barbel 36 20.0 4.2 11.2–28.2 133 72 21–298 1.51 0.17 1.24–2.18 VS1 ± ± ± Nase 23 15.6 1.7 13.5–20.0 44 18 26–92 1.11 0.11 0.95–1.34 ± ± ± Barbel 29 19.9.0 3.3 15.6–27.9 127 66 56–322 1.49 0.10 1.23–1.73 VS2 ± ± ± Nase 21 15.0 1.6 12.8–19.6 40 17 25–99 1.14 0.12 0.96–1.42 ± ± ± Barbel 1 21 17.9 8.9 11.5–43.7 166 344 24–1326 1.55 0.14 1.26–1.83 SNBO1 ± ± ± Nase 1 10 14.8 2.8 11.6–19.6 39 24 19–85 1.12 0.08 0.98–1.22 ± ± ± Barbel 1 18 15.3 2.2 11.8–20.0 56 27 28–130 1.49 0.11 1.32–1.77 SNBO2 ± ± ± Nase 1 7 14.0 3.3 11.0–20.5 35 29 16–99 1.13 0.18 0.92–1.45 ± ± ± 1: Barbels and nases from SNBO group were significantly smaller (p < 0.05) than those from VS group. N = number of fish tagged with PITs; K = condition factor (100 weight/fork length); SD = standard deviation; VS = vertical slot fishway; SNBO = submerged notch with bottom× orifice fishway; barbel = Luciobarbus sclateri; nase = Pseudochondrostoma polylepis. Water 2019, 11, 2362 6 of 14

2.4. Data Analysis During each trial, fish were able to make several ascents. To separate the ascent movements from the exploratory ones, we considered a passage attempt as when a fish reached the second antenna (Figure2, A2). The last detection at antenna 1 (Figure2, A1) was considered as the starting time of the attempt. The attempts in which the fish reached the most upstream antenna (Figure2, A4), were deemed successful; otherwise, they were deemed failures.

2.4.1. Ascent Analysis Of those fish that performed attempts, ascent performance was analyzed using two usual metrics [36–38]: (1) ascent success: percentage of fish that reached A4, in relation to the total number of fish that attempted it. It was analyzed by the chi-square test of independence; and (2) transit time: time taken to move from A1 (last detection) to A4 (first detection) in the fastest successful attempt. Cox proportional hazards regression (PROC, PHREG for SAS) with the Schoenfeld and Martingale residuals test for proportionality [59,60] was used to identify differences in transit time by fishway type and species. In addition, survival analysis based on regression models (PROC, LIFEREG, and “Predict” Macro for SAS; [61]) was used to predict the transit time as a function of the significant covariates and the likelihood of ascent in a given time. The best fitting model was selected using Akaike’s information criterion (AIC) [62]. Additionally, transit time was also expressed in minutes per meter of ascent height (min/m; transit time divided by total water level height ascended), allowing equivalent comparisons to be made between fishways or species. The median was used as the reference value due to the non-normal distribution of the data.

2.4.2. Motivation Analysis Motivation was studied using three specific metrics: (1) attempt percentage: percentage of fish that attempted to ascend in relation to the total number of fish, analyzed using the chi-square test of independence; (2) number of attempts per fish: number of attempts staged by those fish, analyzed via Mann-Whitney test for median comparisons; and (3) attempt rate: proportion of attempts per unit of time, analyzed by Cox proportional hazards regression with Schoenfeld and Martingale test, which stratified the attempts and assessed the influence of fishway type and species. A differentiation between the first attempt (pre-attempt: first attempt in a trial) and the rest of the attempts was considered [38,60]. Water temperature, depth, and fishway discharge were considered invariant during the time of the trials. All statistical analyses were performed using SAS® (Cary, NC, USA) (version 9.4) and Statgraphics Centurion (Statgraphics Technologies, Inc., The Plains, Virginia, USA) (version XVI.II) software.

3. Results Fish groups in each fishway (VS1 vs. VS2, and SNBO1 vs. SNBO2) showed no significant differences in all ascent and motivation metrics (p > 0.05 in all cases). Therefore, data for both groups of fish in the same fishway were merged and processed together as a single group. In addition, the possibility of fatigue or learning during the ascent was analyzed by comparing the different attempts, but no pattern was observed to support those hypotheses.

3.1. Ascent Analysis The ascent success in all cases exceeded 80%, with significant differences between the type of fishways for barbel (χ2 = 4.735, p = 0.032) but not for nase (χ2 = 1.609, p = 0.289) (Table3). The ascent success had no relation with the fish length for both species (p > 0.500 in all cases). Regarding transit time, significant differences were found between types of fishway and species. Barbel needed more time than nase in both fishways (p = 0.052 in VS and p = 0.020 in SNBO), and spent less time in VS than Water 2019, 11, 2362 7 of 14

success had no relation with the fish length for both species (p > 0.500 in all cases). Regarding transit Watertime,2019 significant, 11, 2362 differences were found between types of fishway and species. Barbel needed more7 of 14 time than nase in both fishways (p = 0.052 in VS and p = 0.020 in SNBO), and spent less time in VS than in SNBO (p < 0.001) (Table 3). However, nase spent similar median time in VS and SNBO (p = in0.687; SNBO Table (p < 3).0.001) (Table3). However, nase spent similar median time in VS and SNBO ( p = 0.687; Table3). Table 3. Results of the used metrics: percentage of attempts, number of attempts, ascent success, and Tabletransit 3. timeResults (1.80 of m the head). used metrics: percentage of attempts, number of attempts, ascent success, and transit time (1.80 m head). VS (N = 110) SNBO (N = 56) Metrics BarbelVS (N = 110)Nase Barbel SNBO (N = 56)Nase Metrics Attempt percentage (58/66)Barbel 87.9% (39/44) Nase 88.6% (30/39) Barbel 76.9% (8/17) Nase 47.1% Median number of Attempt percentage (583 /(1–16)66) 87.9% (39 5/ 44)(1–12) 88.6% (30/39) 2 (1–6) 76.9% (8/ 317) (1–6) 47.1% Median numberattempts of attempts 3 (1–16) 5 (1–12) 2 (1–6) 3 (1–6) AscentAscent success (55/58) (55/58) 94.9% 94.9% (38/39) (38/39) 94.8% 94.8% (24(24/30)/30) 80.0%80.0% (7/8) (7/8) 87.5% 87.5% 1 MedianMedian transittransit time 1 (54)(54) 12.5 12.5 min min (37) 8.0 8.0 min min (19)(19) 26.3 26.3 minmin (6) (6) 9.3 9.3 min min MedianMedian transit time per 6.96.9 min/m min/m 4.4 min/m min/m 16.616.6 minmin/m/m 5.25.2 min/m min/m meter of height (1.3–274.5) (1.2–342.7) (4.6–405.3) (2.1–34.4) meter of height (1.3–274.5) (1.2–342.7) (4.6–405.3) (2.1–34.4) 1 :1 Fish: Fish number number for thefor calculusthe calculus of transit of transit time di fftimeersfrom differs the from total number the total of number successful of ascents successful due to ascents some missing due time data in antenna 1. Note: VS = vertical slot fishway; SNBO = submerged notch with bottom orifice fishway; barbelto some= Luciobarbus missing sclateritime data; nase in= antennaPseudochondrostoma 1. Note: VS polylepis = vertical. The numberslot fishway; of fish SNBO is indicated = submerged in brackets, notch except forwith the medianbottom number orifice offishway; attempts barbel and median = Luciobarbus transit time sclateri per meter; nase of height,= Pseudochondrostoma where the range ispolylepis in brackets.. The number of fish is indicated in brackets, except for the median number of attempts and median transit Overall,time per fish meter length of height, showed where a significantthe range is relationshipin brackets. with transit time (p = 0.024). The best fitting predictiveOverall, model fish between length showed fish length a significant and transit relationship time was with log-logistic transit time survival (p = 0. regression.024). The best For fitting barbel, fishpredictive length showed model an between inverse fish relation length with and the tra transitnsit time (the was longer log-logistic fish, the survival less transit regression. time) in Forboth fishwaybarbel, types (p < 0.05) (Figure3 and Table4). For nase, while there were no significant di fferences in VS by fish length (p = 0.981), for SNBO the analysis results were significant (p = 0.016) but not conclusive, due to the low number of successful ascents (Table3).

FigureFigure 3. 3.Predictive Predictive log-logisticlog-logistic survivalsurvival model for the proportion of of fish fish ascending ascending (1 (1 m m of of height height exceeded)exceeded) at at a a given given transit transit timetime asas aa functionfunction of fishfish species and and fork fork leng lengthth (10, (10, 15, 15, and and 20 20 cm) cm) (a (),a ), andand fishway fishway type type and and length length for for barbel barbel (which (which showedshowed significantsignificant didifferences)fferences) (b). Note: Note: VS VS == verticalvertical SlotSlot fishway; fishway; SNBO SNBO= =submerged submerged notchnotch withwith bottombottom orificeorifice fishwayfishway (SNBO); barbel barbel == LuciobarbusLuciobarbus sclaterisclateri; nase; nase= =Pseudochondrostoma Pseudochondrostoma polylepispolylepis.. Nase in in SNBO SNBO are are not not included included due due to to the the small small sample sample size,size, which which would would not not achieve achieve a a reliable reliable predictive predictive model.model.

BasedBased on on this this model model (Figure(Figure3 3and and Table Table4), 4), the the e effectffect could be expressed approximately approximately as as reductionreduction in in transit transit time timeof of 7.5%7.5% forfor barbelbarbel in VS (exp(ββ)) − 11 == exp(exp(−0.078)0.078) − 1 =1 −=0.075)0.075) and and3.4% 3.4% in − − − − inSNBO SNBO per per cm cm increase increase in in fork fork length length (considering (considering the the mean mean value value of of all all fish). fish). As As an an example example of of prediction, it could be said that 50% of barbel with a fork length of 15 cm would ascend 1 m height in 10 min for VS and in 17 min for SNBO. However, if the fork length was 10 cm, the transit time would be 14 min/m and 21 min/m, respectively. Condition factor did not show significant relationships in any case for ascent analysis parameters. Water 2019, 11, 2362 8 of 14

Table 4. Estimation of the parameters of log-logistic survival model (µ = regression intercept; β = fork length, in cm; σ = curve shape of the model) for the proportion of fish ascending at a given transit time as a function of fish length by fishway type (predictive model in Figure3).

Barbel VS SNBO Parameters Coefficient SE p Coefficient SE p Intercept (µ) 3.4601 0.5425 <0.001 3.3816 0.3209 <0.001 Length (β) 0.0784 0.0268 0.0034 0.0350 0.0155 0.0239 − − Shape (σ) 0.4236 0.0487 0.3657 0.0725 Nase VS SNBO Parameters Coefficient SE p-value Coefficient SE p-value Intercept (µ) 1.6243 1.7664 0.3578 5.4887 1.6238 <0.001 Length (β) 0.0028 0.1161 0.9809 0.2365 0.0979 0.0157 − − Shape (σ) 0.6001 0.0882 0.3033 0.1063 Note: SE = coefficient standard error; VS: vertical slot fishway; SNBO = submerged notch with bottom orifice fishway. barbel = Luciobarbus sclateri; nase = Pseudochondrostoma polylepis.

3.2. Motivation Analysis The attempt percentage exceeded 75% in all cases, except for the nase in SNBO (Table3). Nase performed a significantly lower number of attempts in SNBO (χ2 = 11.987; p = 0.001), while barbel showed no differences between fishways (χ2 = 2.168; p =0.074) (Table3). The median number of attempts per fish was higher for barbel in VS than in SNBO (3 vs. 2 attempts respectively; p = 0.0165), whereas there were no significant differences for nase (5 vs. 3 attempts; p = 0.168). Regarding the attempt rate, there were significant differences in relation to the type of fishway (p < 0.001) but not between species (p > 0.05) for both pre-attempt rate and rate of the rest of attempts (Table5 and Figure4). The model fits indicated a significantly lower rate in SNBO than in VS (exp( β) − 1) 100 = 61.4% and 45.1% for pre-attempt rate and rate of the rest of attempts, respectively). This means · that the likelihood of staging an attempt (hazards ratio = exp(β)) in SNBO is 38.6% lower for pre-attempt and 54.9% lower for other attempts.

Table 5. Estimation of the parameters of the Cox proportional hazards models (β: regression coefficient; HR: hazards ratio = exp(β); SE: standard error) for the attempt rate (pre-attempt and rest of attempts) in relation to the type of fishway and species for the reference factors submerged notch with bottom orifice fishway (SNBO) and nase (Iberian straight-mouth nase).

Pre-Attempt Rate Rest of Attempts Rate Parameters β SE p-Value HR β SE p-Value HR ± ± Fishway 0.951 0.189 <0.001 0.386 0.599 0.149 <0.001 0.549 − ± − ± Species 0.595 0.124 Water 2019, 11, 2362 9 of 14 Water 2019, 11, 2362 9 of 14

Figure 4. Kaplan–Meier curves for the proportion of fishfish attempting to ascend over time. Proportion for the pre-attempt rate (a),), andand proportionproportion forfor thethe restrest ofof thethe attemptsattempts ((bb).).

4. Discussion Most riverriver basinsbasins in in the the Iberian Iberia Peninsulan Peninsula have have a Mediterranean a Mediterranean character, character, and therefore and therefore their native their fishnative communities fish communities have evolved have evol andved are and structured are structured according according to these to semiarid these semiarid environments environments [20,63]. These[20,63]. fish These species fish species have developed have developed unique unique life-history life-history strategies, strategies, which which together together with theirwith their high degreehigh degree of rarity of rarity and endemicity, and endemicity, determine determine the high the conservation high conservation interest interest presented presented by these by faunal these communitiesfaunal communities [8], as in [8], other as regionsin other in regions the circum-Mediterranean in the circum-Mediterranean area [12,14]. area Longitudinal [12,14]. Longitudinal connectivity disruptionconnectivity is disruption one of the is main one of alterations the main threateningalterations threatening fish populations fish populations [4,7,18], which [4,7,18], is probablywhich is magnifiedprobably magnified in environmental in environmental scenarios, suchscenarios, as in thesuch Iberian as in the rivers Iberian in the rivers Mediterranean in the Mediterranean area [9]. area The[9]. present work shows that mitigation measures, such as fishways designed according to criteria of theirThe native present fish work species, shows could that reduce mitigation river fragmentation measures, such impacts as fishways on these areas.designed Thus, according the passage to ecriteriafficiency of istheir presented native forfish two species, potamodromous could reduce cyprinids, river fragmentation which are sentinelimpacts specieson these from areas. semiarid Thus, environmentsthe passage efficiency with diff erentis presented swimming for behaviortwo pota (Southernmodromous Iberian cyprinids, barbel andwhich Iberian are sentinel straight-mouth species nase),from semiarid through environments two of the most with common different pool-type swimmi fishwaysng behavior (vertical (Southern slot and Iberian submerged barbel and notch Iberian with bottomstraight-mouth orifice fishways). nase), through two of the most common pool-type fishways (vertical slot and submergedResults notch reveal with that bottom both species orifice easily fishways). overcame both types of fishways. Overall, ascent success exceededResults 80% reveal in all that trials, both with species a median easily transit overcame time both lower types than of 20 fishways. min/m for Overall, barbel ascent and 10 success min/m forexceeded nase, which80% in would all trials, not with imply a anmedian important transit migratory time lower delay than in 20 any min/m case. for These barbel values and are 10 similarmin/m tofor those nase, forwhich congeners would Luciobarbusnot imply an bocagei importantand Pseudochondrostomamigratory delay in any duriense case.in These the Duerovalues River are similar basin (northernto those for Iberian congeners Peninsula) Luciobarbus [36–38 bocagei]. Other and studies Pseudochondrostoma for the close relative durienseBarbus in the barbusDueroin River the Swissbasin Rhone(northern River Iberian showed Peninsul analogousa) [36–38]. transit Other time studies to ours for in pool-typethe close relative fishways Barbus [64]. Inbarbus general, in the fish Swiss size influencedRhone River the showed time needed analogous to overcome transit time the fishway,to ours in with pool-type longer timesfishways for the[64]. smaller In general, fish, whichfish size is consistentinfluenced withthe time other needed fishway to evaluationsovercome the [36 fishway,–38,65]. Longerwith longer fish hadtimes more for the body smaller mass, fish, as well which large is fins,consistent which with are veryother important fishway eval as sourcesuations of [36–38,65]. propulsive Longer forces fish to cross had velocitymore body barriers mass, faster as well [65 large,66]. fins, Nevertheless,which are very the important study reveals as sources significant of propulsi differencesve forces in theto cross variables velocity that barriers define the faster ascent [65,66]. and the motivationNevertheless, between the study fishways reveals and significant species. differenc Nase ascendedes in the both variables types that with define similar the speeds ascent and fasterthe motivation than barbel, between meanwhile fishways the latterand species. ascended Nase faster ascended in VS and both with types higher with percentage similar speeds of success. and Bothfaster species than barbel, presented meanwhile a higher the motivation latter ascended in VS. faster in VS and with higher percentage of success. Both Despitespecies presented the fact that a higher both barbelmotivation and nasein VS. are rheophilic potamodromous cyprinids [16] and usuallyDespite coexist the in fact the samethat both river reaches,barbel and their nase swimming are rheophilic behavior potamodromous is quite different. cyprinids Barbel is a[16] benthic and fish,usually with coexist a robust in the body same and river greater reaches, swimming their sw abilityimming than behavior nase for is the quite same different. fork length Barbel [67 ,is68 a]. Onbenthic the otherfish, hand,with a nase robust is a body water and column greater fish, swimmi with a slenderng ability body than and nase good for swimming the same andfork leapinglength aptitudes,[67,68]. on whichthe other allow hand, them nase to easilyis a water overcome column obstacles fish, with [36 a]. slender body and good swimming and leaping aptitudes, which allow them to easily overcome obstacles [36].

Water 2019, 11, 2362 10 of 14

Differences between our target species could be related to the date of the trials in relation to the reproductive periods of both [19]. Nase fish usually start spawning migration earlier than barbel, with the migratory peak in May, whereas barbel fish start at the beginning of June for the Segura River Basin [69]. Therefore, nase fish were expected to be more active than barbel during trials. However, ascent motivation was similar in both species, except for nase fish in SNBO, which showed lower attempt percentage. The upper water origin for the nase sample in SNBO compared to VS could partly explain the lower motivation for nase group. Colder water temperatures in upper parts of the basin could delay the maturation, and therefore the motivation, compared to the middle part in the main stream, and also the change of water quality from the capture area to the experimental site could influence fish behavior [37]. Moreover, although the difference between SNBO and VS in the experimental fish size was very small, individuals from the first type were significantly smaller, which could also have had an effect on fish motivation. All of our experimental individuals were mature fish [19], but in the case of nase fish, the first size of maturity was very close to the average size of the experimental specimens, which was more obvious in SNBO individuals. Alexandre et al. [70] observed differences in swimming ability for Luciobarbus bocagei population depending on the river stretch of origin, which could be related to their genetic origin, but also to the habitat drivers from each population. Results from our study also showed slight differences in metrics, which could be explained by the origin of the populations and of each target species. Although nase has been completely adapted to the Segura River Basin since its colonization [19], it originally inhabits stretches of high–moderate velocity in their native source from the River, which are very different from the slow waters of the Segura River in the studied fluvial sector. Compared to barbel, it is best adapted to running waters, which could explain the faster transit times observed in the present study. Although the hydraulic design parameters of both fishways were within the usual recommendations for cyprinids [24,32], some slight differences were found between them regarding the volumetric energy dissipation and water velocity. Changes in headwater or tailwater levels modify the hydraulic conditions in the entrance from the ones defined during the design process, causing non-uniform (backwater or drawdown) profiles [33]. During trials, the SNBO presented a more evident backwater profile, where the downstream pools, including the starting pools and the pools between A1 and A2, were more submerged (water drops <0.15 m) than the other pools. This produced lower water velocity in the notches and orifices, and lower volumetric energy dissipation in pools (less than 1 m/s and 100 W/m3), which could have reduced the motivation due to the relationship with velocity in the notches [60,71,72], which would have increased the transit time. Larinier et al. [73] recommends a speed higher than 1 m/s in the notches and slots for most species, and in the order of 2 m/s to 2.4 m/s for large rheophilic fish. Therefore, fishway design projects for upstream migrating fish, specifically for potamodromous cyprinids in semiarid environments such as the Segura River, may provide an opportunity to develop safe, timely, and effective fish passage structures. Results obtained in this field study reveal that both fishway types, if correctly designed and constructed, offer interesting alternatives to mitigate the longitudinal connectivity problems for two sentinel cyprinids from those rivers in semiarid environments. However, further research is necessary to improve the knowledge of the relationships between the behavior and swimming ability of different fish species in the different fishway types and hydraulic scenarios. In fact, a complete and exhaustive fish-based monitoring assessment of the effectiveness of fishways should be an essential part of any project, in order to restore the longitudinal connectivity.

Author Contributions: All authors have contributed substantially to the manuscript development. F.J.S.-R., M.T., and F.J.O.-P. conceptualized, supervised, and administered the project. F.J.B.-C. and F.J.S.-R. designed the applied methodology. F.J.B.-C., L.F.-C., and A.S.-P. conducted the experiments and data collection. F.J.B.-C., A.G.-V., and L.F.-C. analyzed the data. J.V.-C. performed the visualization of this work. F.J.S.-R. wrote the original draft, which was revised by the other authors. Funding: This research was funded by LIFE+ Segura Riverlink, project LIFE12 ENV/1140. Ana Sánchez-Pérez’s contribution was financed by a Ph.D. grant from the Spanish Ministry of Science and Education FPU14/03994. Water 2019, 11, 2362 11 of 14

Ana García-Vega’s contribution was financed by a Ph.D. grant from the University of Valladolid PIF- UVa 2017. Jorge Valbuena-Castro´s contribution was financed by a public Ph.D. grant from Junta de Castilla y León and European Social Fund PIF-2017. Acknowledgments: The authors would like to thank to Agrarian Technological Institute (ITAGRA.CT) for its technical and human support. Conflicts of Interest: The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

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